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Population Fluctuations of Gynaikothrips Ficorum (Marchal, 1908) (Thysanoptera, Tubulifera) and Natural Enemies on Leaf Gall of Ficus Retusa in Algeria

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Population Fluctuations of Gynaikothrips Ficorum (Marchal, 1908) (Thysanoptera, Tubulifera) and Natural Enemies on Leaf Gall of Ficus Retusa in Algeria Arxius de Miscel·lània Zoològica, 17 (2019): 59–71 ISSN:Ziouani 1698– et0476 al. Population fluctuations of Gynaikothrips ficorum (Marchal, 1908) (Thysanoptera, Tubulifera) and natural enemies on leaf gall of Ficus retusa in Algeria Kh. Ziouani, A. Benzehra, L. Saharaoui Ziouani, Kh., Benzehra, A., Saharaoui, L., 2019. Population fluctuations of Gynaikothrips ficorum (Marchal, 1908) (Thysanoptera, Tubulifera) and natural enemies on leaf gall of Ficus retusa in Algeria. Arxius de Miscel·lània Zoològica, 17: 59–71, Doi: https://doi.org/10.32800/ amz.2019.17.0059 Abstract Population fluctuations ofGynaikothrips ficorum (Marchal, 1908) (Thysanoptera, Tubulifera) and natural enemies on leaf gall of Ficus retusa in Algeria. Monthly fluctuations of thrip populations on Ficus retusa were monitored and parasites and predators in Boudouaou, Algeria, were identified. Twenty leaves were collected fortnightly from 30 trees from January to December 2015. The number of eggs increased significantly in August with 11,163 eggs and was slightly higher in October with 11,471 eggs. Presence was rare in spring and winter. The 1st and 2nd larval stages (L1 and L2) overlapped: L1 were present from August to October with 27 and 51 individuals respectively, and L2 were present from August to December with 65 to 186 individuals respectively. Prepupae were active in April and June, reaching 46 and 50 indi- viduals respectively, before increasing to 266 in November. Highest numbers of pupae were observed in June (171) and July (135). The number of adults gradually increased, reaching a maximum of 642 in early December. Two predators were identified: Montandoniola confusa (Hemiptera, Anthocoridae) and Nephus peyerimhoffi (Coleoptera, Coccinellidae). A parasite, Tetrastichus gentilei (Hymenoptera, Eulophidae), was also later identified. Key words: Gynaikothrips ficorum, Ficus retusa, Predators, Parasite, Algeria Resumen Fluctuaciones en las poblaciones de Gynaikothrips ficorum (Marchal, 1908) (Thysanoptera, Tubulifera) y de sus enemigos naturales en las agallas de hojas de Ficus retusa en Argelia. El estudio consiste en la observación de las fluctuaciones mensuales de las poblaciones de arañuelas en Ficus retusa, así como de sus parásitos y depredadores conocidos, en Boudouaou. Para ello, cada quince días se recogieron 20 hojas de cada uno de los árboles seleccionados, durante 12 meses de enero a diciembre de 2015. Aparentemente, el número de huevos aumenta considerablemente en agosto, cuando se registraron 11.163 huevos, valor que se superó ligeramente en octubre, con 11.471 huevos, frente a una ausencia casi total de los mismos en primavera e invierno. Se solapan los estadios larvarios 1 y 2 (L1 y L2): L1 va de agosto a octubre, con 27 y 51 individuos respectivamente, seguido de L2, con 65 y 186 individuos de octubre a diciembre. Las prepupas están activas en abril y © [2019] Copyright belongs to the authors, who license the journal Arxius de Miscel·lània Zoològica to publish the paper under a Creative Commons Attribution 4.0 License, which permits its distribution, and reproduction in any medium, provided the original authors and source, the journal Arxius de Miscel·lània Zoològica, are cited.59 El © [2018] del artículo pertenece al autor o autores; estos autorizan a la revista Arxius de Miscel·lània Zoològica la publicación del artículo bajo la licencia de Creative Commons Reconocimiento 4.0 que permite un uso no restringido, la distribución y la reproducción en cualquier medio, siempre que se citen los autores y la revista. Arxius de Miscel·lània Zoològica, 17 (2019): 59–71 Ziouani et al. junio, cuando alcanzan 46 y 50 individuos, respectivamente, para aumentar hasta 266 en noviembre, si bien muestran valores elevados en junio y julio, con 171 y 135 ejemplares respectivamente. Los individuos adultos aumentan progresivamente hasta llegar al máximo a principios de diciembre, con 642 individuos. Se han identificado asimismo, dos depredado- res: Montandoniola confusa (Hemiptera, Anthocoridae) y Nephus peyerimhoffi (Coleoptera, Coccinellidae) y solo un parásito: Tetrastichus gentile (Hymenoptera, Eulophidae), que aparece al final tras los otros dos depredadores y actúa junto con estos. Palabras clave: Gynaikothrips ficorum, Ficus retusa, Depredadores, Parásito, Argelia Resum Fluctuacions en les poblacions de Gynaikothrips ficorum (Marchal, 1908) (Thysanoptera, Tu- bulifera) i dels seus enemics naturals a les gales de fulles de Ficus retusa a Algèria. L’estudi consisteix en l’observació de les fluctuacions mensuals de les poblacions d’aranyols en Ficus retusa, així com dels seus paràsits i depredadors coneguts, a Boudouaou. Amb aquest objectiu, cada quinze dies es van recollir 20 fulles de cadascun dels arbres seleccionats, durant 12 mesos de gener a desembre de 2015. Aparentment, el nombre d’ous augmenta considera- blement a l’agost, quan se’n van registrar 11.163, valor que es va superar lleugerament a l’octubre, amb 11.471 ous. Durant la primavera i l’hivern es va registrar una absència gairebé total d’ous. Se superposen els estadis larvaris 1 i 2 (L1 i L2): L1 va d’agost a octubre, amb 27 i 51 individus respectivament, seguit d’ L2, amb 65 i 186 individus d’octubre a desembre. Les prepupes estan actives a l’abril i al juny, quan assoleixen 46 i 50 individus, respectiva- ment, i augmenten fins a 266 al novembre, si bé mostren valors elevats al juny i al juliol, amb 171 i 135 exemplars respectivament. Els individus adults augmenten progressivament fins a arribar al màxim al començament de desembre, amb 642 individus. També s’han identificat dos depredadors: Montandoniola confusa (Hemiptera, Anthocoridae) i Nephus peyerimhoffi (Coleoptera, Coccinellidae) i només un paràsit: Tetrastichus gentile (Hymenoptera, Eulophi- dae), que apareix al final després dels altres depredadors i actua juntament amb aquests. Paraules clau: Gynaikothrips ficorum, Ficus retusa, Depredadors, Paràsit, Algèria Received: 11/03/2019; Conditional acceptance: 17/04/2019; Final acceptance: 04/06/2019 Khawla Ziouani, Abdelmadjid Benzehra, Lounes Saharaoui, Department of Agricultural and Forest Zoology, High National School of Agronomy, Avenue Hassen Badi, El–Harrach, 16200 Algiers, Algeria. Corresponding author: Khawla Ziouani. E–mail: [email protected] / [email protected] ORCID: https://orcid.org/0000–0002–3895–2096 Introduction About 6,227 species of Thysanoptera are known worldwide (Mound, 2018), 300 species of which produce galls in various plant species (Ananthakrishnan, 1993; Crespi et al., 1997; Lewis, 1997; Mound, 2003). Forty species of the genus Gynaikothrips (Zimmermann) are cecidophagous or galligenous, and originate from Southeast Asia, but have been described from Africa; they are associated with Moraceae plants and especially infest the ornamental Ficus and fruiting figs causing considerable damage (Mound, 2009; Dang et al., 2014). Among these species, Gynaikothrips ficorum (Marchal), also known as Cuban laurel thrips and G. uzeli (Zimmermann), are considered the most studied species due to their similar morphological traits (Priesner, 1939). 60 Arxius de Miscel·lània Zoològica, 17 (2019): 59–71 Ziouani et al. G. ficorum (Marchal) is a pantropical species introduced to Algeria from Southeast Asia and first recorded by Del Canizo (1945). It prefers leaf–gall onFicus microcarpa L. var. nitida (Urticales, Moraceae) (Priesner, 1939; Alford, 2013; Tree and Wolter, 2009), but in case of abundant infestation, it feeds on other hosts, particularly other genus of Ficus, namely F. axillaris, F. aurea, F. Benjamina, F. elastica, F. retusa, as well as Codiaeum variegatum, Melicocca bijuga, Nicotiana tabacum, Viburnum suspensum and Citrus sp. It has also been found on Eucalysptus sp. in Cuba, Gliricidia in Puerto Rico, Calicarpum sp. in Colombia (Denmark, 1967), and occasionally on orchids (Nixon, 1999). Feeding on tender leaves causes the formation of purplish red spots on the underside of the leaves. These become curled and form galls where G. ficorum matting, oviposition and larval development take place (Mound and Marullo, 1996; Morcos, 1944; Wolcott, 1953). Other pests are also associated with G. ficorum within the leaf galls, such as Chrysomphalus pinnulifer (Diaspididae), Singhiella citrifoli (Aleyrodidae), Greenidea ficicola (Aphididae) (Tawfik, 1967; Paine, 1992; Held et al., 2005; Narrea-Cango et al., 2013; Mifsud et al., 2012; Antonatos et al., 2015). However, several authors have reported the presence of pre- dators on leaf galls such as: Ontandoniola moraguesi, Orius albidipennis, Macrotracheliella laevis, Cardiastethus rugicollis, Anthochoris flavipes, Anthocoris nemoralis (Hemiptera, Anthocoridae), Termatophylum insigne (Hemiptera, Termatophylidae), Cardiastethus rugicollis, Chrysoperla carnea (Neuroptera, Chrysopidae), and Androthrips ramachandrai (Thysanop- tera, Phlaeothripidae). Whereas Adactylidium sp. (Acari), Pleurotropis sp., Tetrastuchus thripophonus, and Tetrastichus gentilei (Hymenoptera, Eulophidae) are considered as parasites of G. ficorum (Dozier, 1926; Wolcott, 1953; Tawfik, 1967; Varadarasan and Ananthakrishnan, 1981; Paine, 1992; La Salle, 1994; Held et al., 2005; Hoddle et al., 2012; Melo et al., 2013; Antonatos et al., 2015). Several studies on insecticidal control (Wolfenbarger, 1946; Wolcott, 1953; Reinert, 1973) confirm that insecticides can be used to control G. ficorum (Held and Boyd, 2008). Systemic insecticides appear to provide better control than broad–spectrum insecticides that are detrimental to natural enemies that potentially
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